cis-trans compensation

Maheshwari S & Barbash DA 2012 Cis-by-trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8:1002597.

  • many protein-coding genes that contribute to incompatibilities between species show signatures of adaptive evolution, including Lhr, which encodes a heterochromatin protein whose amino acid sequence has diverged extensively between Drosophila melanogaster and D. simulans by natural selection
  • we present surprising results that are inconsistent with this coding-sequence-based model
  • we find no evidence that LHR localization differs between D. melanogaster and D. simulans
  • nor do we find evidence that it mislocalizes in their interspecific hybrids
  • Lhr orthologs are differentially expressed in the hybrid background
  • this asymmetric expression is caused by cis-by-trans regulatory divergence of Lhr
  • Takahasi et al. recently found evidence that stabilization of expression levels within a species involves widespread cis- and trans-compensatory mutations that can be detected as incompatibilities between heterospecific regulatory elements in interspecific hybrids
  • the authors also suggest that signatures of adaptive evolution might result from the rapid accumulation of compensatory changes, and thus reflect the maintenance of an existing function rather than the evolution of a novel one
  • to our knowledge Lhr is the first example of cis-by-trans compensatory evolution occurring at an adaptively evolving hybrid incompatibility gene
  • an intriguing possibility is that the rapid evolution of the protein coding region reflects compensatory changes required to maintain an existing regulatory function of Lhr, rather than to alter its protein function